Scale-free Neural and Physiological Dynamics in Naturalistic Stimuli Processing

Abstract

Neural activity recorded at multiple spatiotemporal scales is dominated by arrhythmic fluctuations without a characteristic temporal periodicity. Such activity often exhibits a 1/f-type power spectrum, in which power falls off with increasing frequency following a power-law function: P(f) ∝ 1/f ^β, which is indicative of scale-free dynamics. Two extensively studied forms of scale-free neural dynamics in the human brain are slow cortical potentials (SCPs) – the low-frequency (<5 Hz) component of brain field potentials – and the amplitude fluctuations of alpha oscillations, both of which have been shown to carry important functional roles. In addition, scale-free dynamics characterize normal human physiology such as heartbeat dynamics. However, the exact relationships amongst these scale-free neural and physiological dynamics remain unclear. We recorded simultaneous magenetoencephalography (MEG) and electrocardiogram (EKG) in healthy subjects under resting state and while performing a discrimination task on scale-free dynamical auditory stimuli that followed different scale-free statistics. We observed that long-range temporal correlation (captured by the power-law exponent β) in SCPs positively correlated with that of heartbeat dynamics across time within an individual, and negatively correlated with that of alpha amplitude fluctuations across individuals. In addition, across individuals, long-range temporal correlation of both SCP and alpha-oscillation amplitude predicted subjects’ discrimination performance in the auditory task, albeit through antagonistic relationships. These findings reveal interrelations amongst different scale-free neural and physiological dynamics and initial evidence for the involvement of scale-free neural dynamics in the processing of natural stimuli, which often exhibit scale-free dynamics.

Significance Statement: Many time-varying natural stimuli such as natural soundscapes, speech and music exhibit scale-free dynamics characterized by a 1/f-type power spectrum. In parallel, scale-free neural dynamics are prominent across observational levels in the brain. Two well-established forms of scale-free neural activity are slow cortical potentials and amplitude fluctuations of alpha oscillations. However, it is unknown if they are related. In addition, the inter-beat interval fluctuation of the healthy human heart follows scale-free dynamics, but its relationship with scale-free neural dynamics is not fully characterized. We observed novel relationships between these different scale-free neural and physiological dynamics. Moreover, naturalistic stimuli exhibiting scale-free dynamics modulate scale-free neural dynamics, and baseline characteristics of scale-free neural dynamics predict an individual’s ability to process naturalistic stimuli.